Polymorphism of the major histocompatibility complex (MHC), DAB1 gene was characterized for the first time in the European bitterling (Rhodeus amarus), a freshwater fish employed in studies of host-parasite coevolution and mate choice, taking advantage of newly designed primers coupled with high-throughput amplicon sequencing. Across 221 genotyped individuals, we detected 1-4 variants per fish, with 28% individuals possessing 3-4 variants. We identified 36 DAB1 variants, and they showed high sequence diversity mostly located within predicted antigen-binding sites, and both global and codon-specific excess of non-synonymous mutations. Despite deep divergence between two major allelic lineages, functional diversity was surprisingly low (3 supertypes). Overall, these findings suggest the role of positive and balancing selection in promotion and long-time maintenance of DAB1 polymorphism. Further investigations will clarify the role of pathogen-mediated selection to drive the evolution of DAB1 variation.

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Ecology and Vertebrate Zoology Faculty of Biology and Environmental Protection University of Łódź Łódź Poland

Department of Zoology and Fisheries Czech University of Life Sciences Prague Kamýcká 129 Prague Czech Republic

Institute of Vertebrate Biology The Czech Academy of Sciences Květná 8 603 65 Brno Czech Republic

Italian National Institute for Environmental Protection and Research Via Vitalino Brancati 60 00144 Rome Italy

Laboratory of Experimental Ecology and Aquaculture Department of Biology University of Rome Tor Vergata Via Cracovia 1 00133 Rome Italy

Zobrazit více v PubMed

Agbali M, Reichard M, Bryjová A, et al. Mate choice for nonadditive genetic benefits correlate with mhc dissimilarity in the rose bitterling (Rhodeus ocellatus) Evolution. 2010;64:1683–1696. doi: 10.1111/j.1558-5646.2010.00961.x. PubMed DOI

Brown JH, Jardetzky TS, Gorga JC, et al. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature. 1993;364:33–39. doi: 10.1038/364033a0. PubMed DOI

Callahan BJ, McMurdie PJ, Rosen MJ, et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Cheng P, Yu D, Liu S, et al. Molecular phylogeny and conservation priorities of the subfamily acheilognathinae (Teleostei: Cyprinidae) Zoolog Sci. 2014;31:300–308. doi: 10.2108/zs130069. PubMed DOI

Douda K, Liu HZ, Yu D, et al. The role of local adaptation in shaping fish-mussel coevolution. Freshw Biol. 2017;62:1858–1868. doi: 10.1111/fwb.13026. DOI

Doytchinova IA, Flower DR. In silico identification of sSupertypes for class II MHCs. J Immunol. 2005;174:7085–7095. doi: 10.4049/jimmunol.174.11.7085. PubMed DOI

Gaspar JM. NGmerge: merging paired-end reads via novel empirically-derived models of sequencing errors. BMC Bioinformatics. 2018;19:536. doi: 10.1186/s12859-018-2579-2. PubMed DOI PMC

Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23:254–267. doi: 10.1093/molbev/msj030. PubMed DOI

Jeon HB, Won H, Suk HY. Polymorphism of MHC class IIB in an acheilognathid species, Rhodeus sinensis shaped by historical selection and recombination. BMC Genet. 2019;20:74. doi: 10.1186/s12863-019-0775-3. PubMed DOI PMC

Jiang H, Lei R, Ding SW, Zhu S. Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics. 2014;15:182. doi: 10.1186/1471-2105-15-182. PubMed DOI PMC

Jombart T. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24:1403–1405. doi: 10.1093/bioinformatics/btn129. PubMed DOI

Kaufman J. Unfinished business: evolution of the MHC and the adaptive immune system of jawed vertebrates. Annu Rev Immunol. 2018;36:383–409. doi: 10.1146/annurev-immunol-051116-052450. PubMed DOI

Kelley J, Walter L, Trowsdale J. Comparative genomics of major histocompatibility complexes. Immunogenetics. 2005;56:683–695. doi: 10.1007/s00251-004-0717-7. PubMed DOI

Klein J. Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol. 1987;19:155–162. doi: 10.1016/0198-8859(87)90066-8. PubMed DOI

Klein J, Sato A, Nikolaidis N. MHC, TSP, and the origin of species: from immunogenetics to evolutionary genetics. Annu Rev Genet. 2007;41:281–304. doi: 10.1146/annurev.genet.41.110306.130137. PubMed DOI

Kosakovsky Pond SL, Frost SDW. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol. 2005;22:1208–1222. doi: 10.1093/molbev/msi105. PubMed DOI

Kosakovsky Pond SL, Posada D, Gravenor MB, et al. Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol. 2006;23:1891–1901. doi: 10.1093/molbev/msl051. PubMed DOI

Kumar S, Stecher G, Li M, et al. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC

Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27:2957–2963. doi: 10.1093/bioinformatics/btr507. PubMed DOI PMC

Murrell B, Moola S, Mabona A, et al. FUBAR: a fast, unconstrained Bayesian approximation for inferring selection. Mol Biol Evol. 2013;30:1196–1205. doi: 10.1093/molbev/mst030. PubMed DOI PMC

Murrell B, Wertheim JO, Moola S, et al. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 2012;8:e1002764. doi: 10.1371/journal.pgen.1002764. PubMed DOI PMC

Ottová E, Šimková A, Martin JF, et al. Evolution and trans-species polymorphism of MHC class IIβ genes in cyprinid fish. Fish Shellfish Immunol. 2005;18:199–222. doi: 10.1016/j.fsi.2004.07.004. PubMed DOI

Radwan J, Babik W, Kaufman J, et al. Advances in the evolutionary understanding of MHC polymorphism. Trends Genet. 2020;36:298–311. doi: 10.1016/j.tig.2020.01.008. PubMed DOI

Reichard M, Liu H, Smith C. The co-evolutionary relationship between bitterling fishes and freshwater mussels: Insights from interspecific comparisons. Evol Ecol Res. 2007;9:239–259.

Reichard M, Spence R, Bryjová A, et al. Female rose bitterling prefer MHC-dissimilar males: experimental evidence. PLoS ONE. 2012;7:e40780. doi: 10.1371/journal.pone.0040780. PubMed DOI PMC

Reichard M, Vrtílek M, Douda K, Smith C. An invasive species reverses the roles in a host–parasite relationship between bitterling fish and unionid mussels. Biol Lett. 2012;8:601–604. doi: 10.1098/rsbl.2011.1234. PubMed DOI PMC

Sandberg M, Eriksson L, Jonsson J, et al. New chemical descriptors relevant for the design of biologically active peptides. A multivariate characterization of 87 amino acids. J Med Chem. 1998;41:2481–2491. doi: 10.1021/jm9700575. PubMed DOI

Schwensow N, Fietz J, Dausmann KH, Sommer S. Neutral versus adaptive genetic variation in parasite resistance: Importance of major histocompatibility complex supertypes in a free-ranging primate. Heredity (edinb) 2007;99:265–277. doi: 10.1038/sj.hdy.6800993. PubMed DOI

Sebastian A, Herdegen M, Migalska M, Radwan J. AMPLISAS: a web server for multilocus genotyping using next-generation amplicon sequencing data. Mol Ecol Resour. 2016;16:498–510. doi: 10.1111/1755-0998.12453. PubMed DOI

Seifertová M, Šimková A. Structure, diversity and evolutionary patterns of expressed MHC class IIB genes in chub (Squalius cephalus), a cyprinid fish species from Europe. Immunogenetics. 2011;63:167–181. doi: 10.1007/s00251-010-0495-3. PubMed DOI

Smith C, Reichard M, Jurajda P, Przybylski M. The reproductive ecology of the European bitterling (Rhodeus sericeus) J Zool. 2004;262:107–124. doi: 10.1017/S0952836903004497. DOI

Smith MD, Wertheim JO, Weaver S, Murrell B, Scheffler K, Kosakovsky Pond SL. Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol Biol Evol. 2015;32:1342–1353. doi: 10.1093/molbev/msv022. PubMed DOI PMC

Wang S, Liu C, Wilson AB, et al. Pathogen richness and abundance predict patterns of adaptive major histocompatibility complex variation in insular amphibians. Mol Ecol. 2017;26:4671–4685. doi: 10.1111/mec.14242. PubMed DOI

Won H, Jeon H-B, Kim D-Y, Suk HY. Differential patterns of diversity at neutral and adaptive loci in endangered Rhodeus pseudosericeus populations. Sci Rep. 2021;11:1–12. doi: 10.1038/s41598-021-95385-w. PubMed DOI PMC